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Canine Distemper in Endangered Ethiopian

Wolves
Article in Emerging Infectious Diseases May 2015
Impact Factor: 6.75 DOI: 10.3201/eid2105.141920 Source: PubMed

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RESEARCH

Canine Distemper in Endangered

Ethiopian Wolves
Christopher H. Gordon, Ashley C. Banyard, Alo Hussein, M. Karen Laurenson, James R. Malcolm,
Jorgelina Marino, Fekede Regassa, Anne-Marie E. Stewart, Anthony R. Fooks, Claudio Sillero-Zubiri

The Ethiopian wolf (Canis simensis) is the worlds rarest canid; 500 wolves remain. The largest population is found
within the Bale Mountains National Park (BMNP) in southeastern Ethiopia, where conservation efforts have demonstrated the negative effect of rabies virus on wolf populations. We describe previously unreported infections with
canine distemper virus (CDV) among these wolves during
20052006 and 2010. Death rates ranged from 43% to 68%
in affected subpopulations and were higher for subadult than
adult wolves (83%87% vs. 34%39%). The 2010 CDV outbreak started 20 months after a rabies outbreak, before the
population had fully recovered, and led to the eradication of
several focal packs in BMNPs Web Valley. The combined
effect of rabies and CDV increases the chance of pack extinction, exacerbating the typically slow recovery of wolf
populations, and represents a key extinction threat to populations of this highly endangered carnivore.

nfectious diseases are a major cause of population declines in wildlife (1). Canine distemper virus (CDV;
family Paramyxoviridae, genus Morbillivirus) constitutes
one such threat and has caused outbreaks in a diverse range
of wild mammals: black-backed jackals (Canis mesomelas) (2); lions (Panthera leo) (3); spotted hyenas (Crocuta crocuta) (4); fennecs (Vulpes zerda); rhesus monkeys
(Macaca mulatta) (5); and aquatic species, including Lake
Baikal seals (Phoca sibirica) and Caspian seals (Phoca
caspia) (6). CDV has also affected several threatened carnivores, including the worlds most endangered felid, the
Iberian lynx (Lynx pardinus) (7); the Santa Catalina Island
Author affiliations: Zoological Society of London, London, UK
(C.H. Gordon); University of Oxford, Tubney, UK (C.H. Gordon,
J. Marino, A.-M.E. Stewart, C. Sillero-Zubiri); Animal and Plant
Health Agency, New Haw, UK (A.C. Banyard, A.R. Fooks);
Ethiopian Wolf Conservation Programme, Bale Robe, Ethiopia
(A. Hussein, J. Marino, A.-M.E. Stewart, C. Sillero-Zubiri);
Frankfurt Zoological Society, Addis Ababa, Ethiopia
(M.K. Laurenson); University of Redlands, Redlands, California,
USA (J.R. Malcolm); Ethiopian Wildlife Conservation Authority,
Addis Ababa (F. Regassa); University of Liverpool, Liverpool, UK
(A.R. Fooks)
DOI: http://dx.doi.org/10.3201/eid2105.141920
824

fox (Urocyon littoralis catalinae) (8); and the Amur tiger

(Panthera tigris altaica) (9). Rapidly expanding human
populations increase domestic dog contact with wild canids (10,11), exacerbating the risk for disease transmission
(12,13). CDV infections in different species are serologically indistinguishable due to the existence of a single stereotype of the virus.
The Ethiopian wolf (Canis simensis) is recognized as
the rarest canid species in the world and as the most threatened carnivore in Africa. Fewer than 500 adult and subadult wolves remain in half a dozen suitable Afroalpine
habitat ranges (14). The largest population is in the Bale
Mountains National Park (BMNP) in southeastern Ethiopia, where wolf populations reach densities of up to 1.4
adults and subadults/km2 (15). On average, family packs
contain 6 adult and subadults (range 220) and protect a
home range of 6 km2 (16). Such high wolf densities, large
packs, and intense social behaviors increase the risks for
disease transmission (17). As a result of rabies outbreaks
during 19911992 (18), 2003 (19), and 20082009 (20),
wolf subpopulations in BNMP were dramatically reduced
by 45%75% .
Serologic evidence for CDV within wolf populations has been reported (21); of 30 samples tested during
19891992, a total of 9 (30%) were seropositive for CDV.
This finding among wild mammal populations shows that
survival rates among animals with canine distemper (CD)
infection can be high, as most clearly evidenced in populations of rare or threatened species that are likely to be closely monitored by field conservation efforts. Furthermore,
it is well established that the virulence of CDV can vary
greatly depending on the infecting virus strain, the immunologic competence of the infected host, and the presence of
preexisting infections that can be exacerbated by the immunosuppressive effect of infection with a morbillivirus (22).
Population viability analyses have been used to predict the effect of epizootics on wolf populations, and the
findings suggest that periodic CD epizootics would play a
relatively minor role in population persistence, even when
modeled together with rabies (23,24). However, estimated
CD-associated death rates in these models were low (15%
20%), and a caveat of the study findings was that the effect on wolf populations should be reassessed if death rates

Emerging Infectious Diseases www.cdc.gov/eid Vol. 21, No. 5, May 2015

Canine Distemper in Endangered Ethiopian Wolves

were >40% (23). These models predicted that populations

could recover from outbreaks of rabies or CDV, but if the
interval between disease outbreaks was <30 months, the
likelihood of local extinction would be high in the absence
of low-coverage parenteral vaccination campaigns (25).
To confirm whether CDV poses an extinction threat to
Ethiopian wolves, we examined the effect of CDV infection on pack and population dynamics during 2 CD epizootics in BMNP and quantified their effect on the wolf
populations. We investigated the source of CD epizootics
in village dogs close to the geographic onset of the outbreaks and compared CD-associated deaths between domestic dogs and wild canids.
Animal care and use protocols for the ethical handling
of domestic dogs in this study were approved by the Oxford
University Zoology Ethical Review Committee (case no.
ZERC040905). Animal care and use protocols adhere to
the Animals (Scientific Procedures) Act regulations (1986)
in the United Kingdom. Furthermore, all animal handling
protocols were approved by the Ethiopian Wildlife Conservation Authority.
Materials and Methods
The BMNP, in south-central Ethiopia (654N, 3942E),
contains the largest remaining continuous range of Afroalpine habitat (26), upon which Ethiopian wolves are
dependent. Wolves in BMNP are found in 3 major subpopulations, all linked by narrow geographic corridors:
Morebawa, the Web Valley, and Sanetti Plateau (Figure 1).
Wolves are present throughout the Afroalpine range but occur in high densities in these subpopulations.
Since 2001, the Ethiopian Wolf Conservation Programme has closely monitored focal wolf packs in all 3
subpopulations. A total of 18 focal wolf packs were intensively monitored in the 3 areas; 41 packs in other areas,
including the Worgona Valley and Chafadalacha, were
monitored less intensively (Figure 1) (27). Time series of
wolf pack densities of the focal packs in Sanetti and the
Web Valley were calculated at 6-month intervals; intensive
monitoring data and disease information were incorporated
in the time series. Wolves up to 1 and 12 years of age are
classified as juveniles and subadults, respectively; full adult
physical appearance and sexual maturity are attained at 2
years of age. We calculated long-term population trends
annually and presented them densities of adult and subadult
wolves around the time of breeding. To calculate densities,
we considered the area occupied by each population as the
95% kernel of all wolf sightings during the breeding season
(OctoberMarch).
Intensive monitoring enabled the timely recovery of
wolf carcasses and the detection of disease epizootics,
and detailed pack composition data enabled the recognition of missing wolves, even when their carcasses were

Figure 1. Bale Mountains National Park in Ethiopia, showing

location of wolves that died during the 20052006 and 2010 canine
distemper virus outbreaks in Worgona Valley and Sanetti Plateau
and the location of Ayida village, the source of the outbreaks.

not found. Wherever possible, wolf carcasses were subjected to detailed postmortem examination and sampling,
following established protocols (28). Samples, including
lymph node, lungs, spleen, and brain tissue, were collected
when possible.
Interviews were conducted in 62 households in Ayida
village, 2 km from a wolf pack in Worgona Valley, after
reports of a disease outbreak in the area. Domestic dogs
that were suspected to have recovered from the virus were
captured, and blood samples were obtained for testing.
We analyzed tissue samples for the presence of CDV
antibody by using a semiquantitative solid-phase ELISA
(ImmunoComb; Biogal, Galed Labs, Galed, Israel). Where
possible, we macerated tissues and extracted total cellular
RNA by using Trizol (Invitrogen, Carlsbad, CA, USA).
Reverse transcription PCR was performed, and a segment
of the phosphoprotein (P) gene was generated as described
previously (29). We sequenced positive reaction products
of the correct size (429 bp) in their entirety with primer
sequences removed from the consensus. We amplified a
section of the hemagglutinin (H) gene in the same manner,
using H-specific primers (CDVF1 5TTAGGGCTCAGGTAGTCCAACA 3 to CDVR1 5 GACAAGGCCGACTCCAGACAA 3) to yield a 1,122-bp product. P gene and
H gene data were aligned with available data by using
MEGA6 (30). In all cases, assessing statistical significance
using 2 values was done with degrees of freedom = 1.

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RESEARCH

Results
CDV Outbreak 20052006

In July 2005, a total of 65 domestic dog deaths were reported in Ayida village (Figure 1), which was just 2 km
from the nearest wolf pack in Worgona Valley. In 62
households surveyed, 49% (65/132) dogs owned by villagers had died. Owners commonly reported that infected
dogs showed symptoms consistent with a CDV infection,
including ocular discharge, convulsive head nodding, loss
of appetite, and death. An additional 28% (37/132) of the
dogs had been sick but recovered, implying CDV infection
in 77% (102/132) of the village dogs. Of 16 serum samples
collected from dogs that had recovered, 9 (56%) were positive for CDV antibodies by ELISA.
On September 15, 2005, a wolf with hind leg ataxia,
hunching of the back, hair loss, and lethargy was observed
in Worgona Valley. On September 21, a wolf carcass was
discovered, and in December, a juvenile carcass found. In
addition, 7 known wolves disappeared from 4 study packs
in the Worgona Valley during SeptemberDecember. In
total, 9 of 19 wolves died or disappeared, resulting in a presumed 47% death rate among adult and subadult wolves
across 4 packs.
In November 2005, a known female wolf emigrated
from Shiya pack in Worgona to Garba Guracha pack in Sanetti, 5 km to the east, and in January 2006, a wolf carcass
was discovered in the Garba Guracha pack. During JanuaryApril, 13 additional carcasses were recovered in Sanetti (Figure 1), and 10 wolves were observed with clinical
symptoms consistent with CDV infection; 4 of the wolves
recovered and survived the outbreak. In addition to the 14
wolves that were confirmed dead, 17 other known wolves
disappeared from Sanetti during the same period (Table
1), bringing the suspected death rate to 54% (31/58 known
wolves) among the 9 packs. Death rates were higher among
subadults (83%) than adults (34%). Samples were collected
from 3 of 14 carcasses; 2 had positive test results.
CDV Outbreak 2010

In April 2010, 3 wolf carcasses were discovered in Web

Valley and Morebawa (Figure 1), and during JulyAugust,

9 more were discovered. In September, 5 carcasses were

found in Chafadalacha (30 km from Morebawa), and in
November, 5 were detected in Sanetti (25 km from Web
Valley). In total, 31 carcasses were recovered, and 7 samples were collected for analysis. In addition, 3 domestic
dog carcasses were recovered.
In Web Valley, during AprilAugust 2010, a total of 8
wolves were found dead, and another 13 disappeared and
were presumed dead, indicating an estimated death rate
of 68% (21/31 known wolves from 7 packs) (Table 2). In
Sanetti, 8 carcasses were recovered, and 19 more wolves
went missing during OctoberDecember 2010, indicating
a death rate of 43% (27/63 known wolves from 7 packs)
(Table 2). In Morebawa, 5 wolf carcasses were found, and
11 wolves went missing during MayAugust, indicating a
death rate of 47% (16/34 from 6 packs). In focal areas, the
death rate among subadult wolves (87%, 20/23) was higher
than that among adults (39%, 28/71); the death rate among
juvenile wolves was 93% (27/29). Ten additional carcasses
were recovered in nonfocal wolf areas, such as Chafadalacha and Central Peaks.
For the 2 CDV outbreaks combined, the death rates
among subadult (85%) and adult (38%) wolves were significantly higher than the expected annual natural death
rate of 15% (19) (21 = 42.98, N = 106, p<0.001) and (21
= 175.69, N = 46, p<0.001) respectively, but significantly
more subadults than adults died or disappeared (21 = 28.45,
N = 152, p<0.001). The death rate among juvenile wolves
(93%) during the 2010 CDV outbreak was significantly
higher than the expected annual natural death of 37% (15)
(21 = 39.16, N = 29, p<0.001).
CD Diagnosis

An amplicon for the P gene could be amplified from only

1 sample among those analyzed from the 20052006 outbreak. This sequence grouped phylogenetically with sequences reported for isolates from domestic dogs in the
United States and Germany (Figure 2, panel A). Three
postmortem samples from the 2010 outbreak were positive for the CDV P gene or the H gene, and the sequences
aligned most closely with isolates from domestic dogs in
Japan (Figure 2).

Table 1. Age and sex distribution of Ethiopian wolves in focal packs monitored in Sanetti Plateau, Ethiopia, before, during, and after a
20052006 outbreak of canine distemper virus
November 2005, before the outbreak
April 2006, during the outbreak
November 2006, after the outbreak
Adult, Adult,
Adult, Adult,
Adult, Adult,
Focal pack
M
F
Subadult
Total
M
F
Subadult Total
M
F
Subadult Total
Badagassa
4
3
3
10
2
2
0
4
2
2
0
4
Batu
3
2
4
9
2
2
0
4
2
2
0
4
BBC
4
1
7
12
4
1
3
8
2
1
0
3
Garba Guracha
2
2
4
8
2
1
1
4
2
1
1
4
Nyala
3
3
2
8
1
1
1
3
1
1
1
3
Quarry
3
2
3
8
3
1
2
6
3
1
2
6
Bilisa
2
1
0
3
2
1
0
3
2
1
0
3
Total
21
14
23
58
16
9
7
32
14
9
4
27
826

Emerging Infectious Diseases www.cdc.gov/eid Vol. 21, No. 5, May 2015

Canine Distemper in Endangered Ethiopian Wolves

Table 2. Age and sex distribution of Ethiopian wolves in focal packs monitored in Sanetti Plateau and Web Valley, Ethiopia, before,
during, and after a 2010 outbreaks of canine distemper virus
April 2010, before outbreaks
November 2010, during outbreaks
April 2011, after outbreaks
Adult, Adult,
Adult, Adult,
Adult, Adult,
Focal pack
M
F
Subadult Total
M
F
Subadult Total
M
F
Subadult Total
Sanetti Plateau
Badagassa
3
1
3
7
5
2
1
8
3
1
0
4
Batu
4
2
0
6
3
1
0
4
4
1
0
5
BBC
11
3
3
17
7
2
1
10
4
2
1
7
Garba Guracha
4
1
3
8
4
1
2
7
4
1
1
6
Nyala
2
3
2
7
2
1
0
3
1
1
0
2
Quarry
5
3
3
11
4
3
0
7
4
3
0
7
Bilisa
3
2
2
7
3
2
2
7
4
1
0
5
Total
32
15
16
63
28
12
6
46
24
10
2
36
Web Valley
Darkeena
1
1
0
2
0
0
0
0
0
0
0
0
Mulamu
3
2
1
6
0
0
0
0
0
0
0
0
Meggity
3
1
0
4
2
1
0
3
1
1
0
2
Kotera
1
0
0
1
0
0
0
0
0
0
0
0
Sodota
2
2
6
10
1
1
0
2
0
0
0
0
Alandu
3
2
0
5
3
1
0
4
3
1
1
5
Tarura
2
1
0
3
2
1
0
3
2
1
0
3
Total
15
9
7
31
8
4
0
12
6
3
1
10

CDV Effects on Population and Pack Dynamics

Between 2002 and 2013, focal packs in the Sanetti subpopulation were affected by 2 CDV epizootics (20052006 and
2010), but no rabies epizootics were observed. Wolf numbers fluctuated in Sanetti in response to CDV infection; the
interepizootic interval was 4 years (Figure 3). An immediate lull in population growth followed both epizootics.
In 2006, two Sanetti packs (BBC and Lencha) coalesced
to form 1 pack, meaning, in essence, that 1 pack became
extinct. Breeding success during or immediately after the
epizootics was also affected. During 20052006, only 4
(44%) focal packs in Sanetti bred; during 20062007, only
3 (38%) bred; and during 20102011, only 4 (57%) bred.
In 20052006 in Sanetti, only 4 pups in total survived from
3 packs, but in February during the epizootic, all 4 pups
in a fourth pack, Badagassa, died. The remaining 5 packs
in Sanetti did not breed that season. Breeding remained
suppressed in the 20062007 breeding season: only 3 of
8 packs produced pups, of which 10 survived to independence at 6 months of age. During the 20102011 breeding
season, 3 of 7 focal packs did not breed; another 2 packs
bred but lost their pups before emergence at 3 weeks of
age. Four of 9 pups from the other 2 packs died before they
reached independence.
Subsequent to this initial 2-year lull in reproduction,
wolf numbers recovered strongly: by the second outbreak
in 2010, wolf numbers and wolf density in Sanetti had surpassed pre-CDV outbreak levels. The combined wolf density for the 7 focal packs in Sanetti more than doubled during 20072010 (Figure 3).
During 20022013, Web Valley wolf packs were affected by rabies epizootics in 2003 and 20082009 and
by an CDV epizootic in 2010 (Figure 4). Death rates were
62% (19) and 59% (39/66), respectively, for the 2 rabies

epizootics and 68% for the CDV epizootic. Four of 7 Web

Valley packs, including 86% of the subadult wolves that
were born during the 20082009 breeding season, were
eradicated by the CDV epizootic. Two new packs formed
in the Web Valley in 2012.
Discussion
CDV Diagnosis

The detection of CDV-associated deaths among populations of rare Ethiopian wolves is of paramount significance for their effective protection and survival. Alongside the ongoing threat from rabies, deaths from CD
highlight the real and present threat that emerging viral
diseases pose to these endangered carnivores. Molecular
typing of viral pathogens is of great utility in identifying and managing threats to susceptible populations. The
phylogenetic clustering of wolf-derived CDV isolates
with domestic dogderived isolates from geographically
distinct areas is not surprising. CDV isolates were originally reported to cluster geographically, however, increased reporting and genetic analysis of CDV isolates
has shown that translocation of animals, often internationally, can spread the virus globally. Thus, geographically
distinct viruses are often found to cluster (22). Furthermore, data for CDV isolates are scarce, and our epidemiologic understanding of this virus remains unclear in the
absence of genetic data.
CDV Effects on Population and Pack Dynamics

The detailed death information gathered from both epizootics contradicts the predictions of previous population viability analysis models, which were determined on the basis of lower estimated CDV death rates (15%20%). Those

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RESEARCH

models indicated that CDV would have little effect on wolf

population persistence or pack size (23,24). However, the
observed death rates in our study were 24 times higher
than those in the earlier studies (23). When compared with
the effect of natural death rates of 15% per year for subadult and adult wolves (19), the high death rates observed

in our study can rapidly alter population and pack dynamics. The missing subadult and adult wolves in Sanetti in
20052006 (29%) and 2010 (35%) and in Web Valley in
2010 (42%) represented more than the 15% natural death
rate, providing further confirmation that these missing
wolves had died from CD.

Figure 2. Phylogenetic neighbor-joining trees of canine distemper virus (CDV) isolates from samples collected during outbreaks in
2006 and 2011 (A) and 2010 (B). Evolutionary analyses were conducted in MEGA6 (30). A) Tree constructed using the phosphoprotein
gene (331 nt). Evolutionary distances were computed using the Kimura 2-parameter method and are in the units of the number of base
substitutions per site. The analysis involved 45 nt sequences and a total of 331 positions in the final dataset. B) Tree constructed by using
the hemagglutinin gene (1,334 nt). Bootstrap values (10,000 replicates) are indicated at relevant nodes. Black dot indicates Ethiopian
wolf samples. Species from which the viruses were isolated are indicated by the following abbreviations: Am, Ailuropoda melanoleuca
(giant panda); Cf, Canis familiaris (dog); Cs, Canis simensis (Ethiopian wolf); Hu, human; Mma, Martes martes (European marten); Ml,
Mustela lutreola (European mink); Mm, Meles meles (badger); Nv, Neovison vison (American mink); Om, Otocyon megalotis (bat-eared
fox); Ple, Panthera leo (lion); Plo, Procyon lotor (raccoon); Pp, Panthera pardus (black leopard); Ps, Phoca sibirica (Baikal seal); Pv, Phoca
vitulina (harbor seal); Xx, species unidentified. Country of sample origin are indicated as follows: CN, China; DK, Denmark; ET, Ethiopia;
FL, Finland; GE, Germany; GL, Greenland; HU, Hungary; IT, Italy; JP, Japan; NLD, the Netherlands; RU, Russia; RSA, South Africa; TU,
Turkey; TZ, Tanzania. TC denotes where isolates have undergone extensive tissue culture passage. Phylogenetic outgroups are indicated
as follows: PPRV, peste des petits ruminants virus; PDV, phocine distemper virus; and MeV, measles virus.
828

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Canine Distemper in Endangered Ethiopian Wolves

Figure 3. Adult and subadult Ethiopian wolf population in Sanetti

Plateau, Ethiopia, 20022013. Dots indicate wolf population
estimates at different time points; arrows indicate canine
distemper virus outbreaks in this study.

Death rates for wolves with CD were comparable to

those for dogs in Ayida village. The genetic identity of the
virus and the close proximity between the village and wolf
habitat makes it almost certain that the village dogs were
the source of the 20052006 epizootic among wolves; this
finding supports the assertion that CDV is transmitted to
wild canids by domestic dogs (12). Some dogs in Ayida recovered from CD, and the number of surviving dogs combined with the number of dead dogs suggests that the prevalence of CDV infection during the epizootic was much
higher than the reported number of deaths. Wolves can also
survive exposure to CDV, as evidenced by the detection
of a CDV seropositive wolf in 2011 and the detection of
seropositive wolves in 19891992 (21).
Once disease is transmitted from a domestic dog to
an individual wolf, the intense social behavior of wolf
packs enables pathogens to spread almost instantly within
the pack. Adjacent packs interact at territorial boundaries,
permitting further transmission through the population.
However, the 2 epizootics in this study showed different
transmission patterns across subpopulations (Figure 1).
The 20052006 epizootic spread a relatively short distance
from the lower density wolf habitats in Worgona Valley to
the adjacent high-density habitats in Sanetti, where the disease died out. In contrast, the 2010 epizootic moved temporally and geographically from Morebawa to Web Valley
and Sanetti, crossing through geographic bottlenecks and
areas of lower wolf density between these subpopulations.
Interpack contact rates are reduced by low pack connectivity within geographic bottlenecks, reducing the probability
of disease transmission. This fact reinforces the severity of
the 2010 epizootic, which left 64 wolves dead or missing
from the 3 focal subpopulations. Monitoring efforts were
less intense in the nonfocal, lower density wolf areas, so
it was difficult to gauge death in these areas. The reported
losses from focal packs, combined with unknown deaths

from lower density areas, suggest that this was the single
most catastrophic disease event for Ethiopian wolves reported to date; the spread of CDV to all areas of BMNP
caused losses that outnumber reports from all previous rabies epizootics (1820).
CDV had a considerable effect on younger wolves:
death rates among subadults were >2 times higher than
those among adults. Lower death rates in adult wolves will
aid recovery of packs by keeping breeding units (packs) intact, assuming survival of at least 1 adult female. Although
juvenile wolves usually have natural death rates of 37%
during high wolf density periods and 29% during periods
of population recovery (15), juvenile death rates were 3
times these levels after the 2010 epizootic. Lower death
rates among adult wolves may reflect previous low-level
exposure, and thus immunity.
Although the mechanism by which CDV affects reproduction is uncertain, both CDV outbreaks clearly affected
breeding success and pup survival in Sanetti. In periods of
high wolf densities, 75% of packs typically breed successfully, and during periods of population recovery, 83% of
packs typically breed successfully (15); however, <50%
of Sanetti packs bred successfully immediately after both
CDV epizootics. After this lull, breeding was not impaired,
and once the juveniles were recruited into the population,
growth rates were rapid in Sanetti: wolf densities doubled
over a 3-year period. With the exception of the 2 packs
that coalesced, all breeding packs in Sanetti were maintained, and at least 1 adult female survived in each pack.
Four years after the 20052006 outbreak, wolf densities
had recovered above pre-outbreak levels, and signs suggest
a similar outcome following the 2010 outbreak.
Ethiopian wolf populations can recover from CDV
epizootics, but the capacity to recover will be impaired
when intervals between epizootics are short, as was seen
in Web Valley. The brevity of the second interepizootic interval (20 months) meant that wolf numbers had only just
started to recover following the 20082009 rabies epizootic
before the CDV epizootic began. After the 2010 CDV outbreak, death rates were high: 4 of 7 packs were eradicated.
These pack extinctions confirmed modeling predictions
that the probability of pack extinctions greatly increases as
the length of the interepizootic period decreases (23). Although concurrent rabies and CDV infections likely caused
these extreme death scenarios in Web Valley wolves, there
is evidence of high death rate CDV epidemics in lions coinciding with high levels of Babesia spp. infection resulting
from climatic extremes (31); thus, other factors should be
fully explored.
The loss of breeding units can slow population
growth because it is rare for packs of Ethiopian wolves
to split (32), even though large litter sizes and high juvenile survival may occur following a decrease in population

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Figure 4. Density of adult and subadult Ethiopian wolf population

in Web Valley, Ethiopia, 20022013. Dots indicate wolf
population estimates at different time points; arrows indicate
known rabies epizootics and canine distemper virus outbreaks in
this study. Of 7 wolf packs in Web Valley, 4 went extinct after the
2010 canine distemper virus outbreak; in 2011, two new packs
formed in the area.

density (15,33). Dispersal movements are constrained by

the scarcity of suitable, unoccupied habitat, although some
subordinate females disperse once recruited to adult status
(32). Packs will expand their territory if opportunities arise,
usually following the disappearance of a neighboring pack
(34). After the 2010 CDV epizootic, available habitat in
optimal Afroalpine areas was abundant in Web Valley, and
in 2012, two new packs formed (Figure 4), hinting at the
resilience of this species. Several of the founder members
of these new packs came through the corridor from Morebawa and joined surviving solitary wolves from extinct
Web Valley packs. This finding confirms that corridors facilitate migration and recovery after epizootics (35), and
such migration is critical for minimizing genetic drift from
bottlenecks (36). Such mechanisms indicate that individual
wolves take advantage of breeding opportunities and low
population density, filling available habitat to form new
packs. The size and structure of the BMNP wolf population lends robustness to wolf numbers and provides greater
resilience against disease catastrophes (23).
Conservation Implications

CDV is a major threat to the persistence of some threatened carnivore populations, including the Ethiopian wolves.
Long-term disease management plans are vital for conservation of susceptible species, and vaccination of host and target
populations remains a key strategy for disease management
(37,38). Even with incomplete CDV control in domestic
dogs, any reduction in disease incidence should have a beneficial effect on the persistence of a wild endangered species.
Population viability models indicate that disease-induced population fluctuations and extinction risks can be
markedly reduced by the vaccination of a small proportion
of wolves (23,25). However, CDV vaccines for wild species
830

are not currently at the same stage of development as rabies

vaccines. In particular, although licensed for domestic species, live attenuated CDV vaccines can cause adverse reactions in wildlife species. Monovalent canarypox-vectored
CDV recombinant vaccines hold the greatest promise for
protection of wild canids against CDV (39), and trials of the
Nobivac D and P antigens have also been conducted on wildlife (40), with no adverse reactions. The high prevalence of
CDV in the surrounding domestic dog population and the
apparent frequent incursion of CDV into the BMNP wolves
makes finding new disease control strategies all the more urgent, particularly for smaller wolf populations, among which
extinction probabilities are even higher with any reduction
in interepizootic periods (23). The extent of knowledge regarding CDV and its effects is clearly demonstrated in the
well-monitored Ethiopian wolf populations, resulting in suggested conservation solutions that are far reaching in their
potential application to other susceptible threatened carnivore species.
Acknowledgments
We are grateful to the Ethiopian Wildlife Conservation
Authority and Bale Mountains National Park for permission to
work in Bale. This manuscript was greatly improved by
comments from Richard Kock and Tim Coulson.
The Ethiopian Wolf Conservation Programme is chiefly
funded by the Born Free Foundation and the Wildlife
Conservation Network.
Dr. Gordon is the Kenya Country Manager for the Zoological Society of London. His current areas of focus are antipoaching efforts, protected area support, and biodiversity monitoring.
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Address for correspondence: Ashley C. Banyard, Animal and Plant
Health Agency, Woodham Lane, Weybridge KT15 3NB, UK; email:
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